Rodriguésia 68(5): 2001-2017. 2017 http://rodriguesia.jbrj.gov.br DOI: 10.1590/2175-7860201768530
Review Article / Artigo de Revisão Defaunation as a trigger for the additional loss of plant species in fragmented landscapes: considerations on the state of Espírito Santo, southeastern Brazil
Ana Carolina Srbek-Araujo1,2,4, Ariana Pignaton Gnocchi1, Lillian Jardim Guimarães1 & James Joseph Roper3
Abstract Here we present a brief review on how the loss of fauna can cause a concomitant loss in plant diversity in the state of Espírito Santo, focusing on the context of current habitat loss and fragmentation and the importance of the mutualistic interactions between animals and plants. We discuss the main groups of fauna that are involved in pollination and seed dispersal, especially those that are found in the state of Espírito Santo. These ecological processes were selected due to their relevance for population dynamics and population genetics of plants. In Atlantic Forest, important pollinators include a variety of insects (especially bees), along with many species of birds and bats. Seed dispersers also include many taxonomic groups, from ants to large mammals. Each of these groups contribute in their own unique and complementary, rather than redundant, way. Habitat fragmentation causes a variety of problems for habitat integrity and the reduction of species diversity, and smaller fragments tend to support fewer species and smaller populations. As a consequence, pollinators and seed dispersers are lost or their activity is reduced, thereby reducing even further the reproductive success of the plants, leading to a vicious cycle of reduction of species diversity. Key words: animal-plant interaction, fragmentation, habitat loss, pollination, seed dispersal. Resumo O presente trabalho apresenta uma breve revisão sobre como a perda de fauna pode causar a perda concomitante de diversidade vegetal no estado do Espírito Santo, considerando o cenário atual de perda e fragmentação de habitats e a importância das interações mutualísitcas entre animais e plantas. Foram considerados os principais grupos zoológicos envolvidos na polinização e na dispersão de sementes, especialmente aqueles com ocorrência no estado do Espírito Santo. Estes processos ecológicos foram selecionados devido à sua relevância na dinâmica e a genética populacional das plantas. Na Mata Atlântica, importantes polinizadores incluem uma variedade de insetos (especialmente abelhas), juntamente com muitas espécies de aves e morcegos. Os dispersores de sementes também abrangem muitos grupos taxonômicos, desde formigas até grandes mamíferos. Cada um desses grupos contribui de maneira única e complementar, mais do que de forma redundante. A fragmentação de habitats compromete a integridade do habitat e reduz a diversidade de espécies, ressaltando que fragmentos menores tendem a suportar menos espécies e menores populações. Como consequência, os polinizadores e os dispersores de sementes são perdidos ou sua atividade é reduzida, diminuindo ainda mais o sucesso reprodutivo das plantas, levando a um círculo vicioso de redução da diversidade de espécies. Palavras-chave: interação animal-planta, fragmentação, perda de habitat, polinização, dispersão de sementes.
1 Universidade Vila Velha - UVV, Lab. Ecologia e Conservação de Biodiversidade (LECBio), Prog. Pós-graduação em Ecologia de Ecossistemas, R. Comissário José Dantas de Melo 21, Bairro Boa Vista, 29102-920, Vila Velha, ES, Brazil. 2 Instituto SerraDiCal de Pesquisa e Conservação, Belo Horizonte, MG, Brazil. 3 Universidade Vila Velha - UVV, Lab. Dinâmicas Populacionais e Conservação de Vertebrados (DPeC), Prog. Pós-graduação em Ecologia de Ecossistemas, R. Comissário José Dantas de Melo 21, Bairro Boa Vista, 29102-920, Vila Velha, ES, Brazil. 4 Author for correspondence: [email protected] 2002 Srbek-Araujo AC et al.
Introduction Espírito Santo at the time of the early Espírito Santo is one of the four states in traveler naturalists southeastern Brazil, being entirely inserted in The eastern Brazilian state of Espírito the Atlantic Forest ecoregion. The colonization Santo comprises a wide variety of native animals of the capixaba (the local name for the region that fascinated and interested experts since the and people from Espírito Santo) territory early traveler naturalists. Travel notes by prince began in 1535, but the region was essentially Maximilian von Wied-Neuwied during his travels unexplored economically until the half of the in Brazil at the beginning of the 19th century 19th century (Franceschetto 2014). Despite this (in his writings “Viagem ao Brasil nos anos de delay in colonization, natural vegetation in the 1815 to 1818”) describe encounters with a great state suffered from an intense deforestation and diversity of birds in his travels in where today lays forest degradation, and as a consequence of which the state of Espírito Santo, including gulls, herons natural areas are currently restricted to less than and egrets, swallows, shorebirds, ducks, macaws, 13% of their original cover (FSOSMA & INPE parrots and parakeets, toucans, woodpeckers, 2016). Habitat loss and fragmentation, associated hawks, curassows and guans, trogons and brightly with hunting and other anthropic activities (e.g., colored tanagers among many more. In addition, roadkills and introduction of exotic species), lead he also wrote about the frogs, sea turtles, caiman to the current situation of decline and loss of and snakes, a variety of species of monkeys, wildlife in Espírito Santo. A total of 753 species of tapirs, deer, peccaries, porcupines, cats and plants (Simonelli & Fraga 2007) and 197 species manatees, as well as beetles and many kinds of of animals are threatened in the state, and 11 butterflies, all within the state of Espírito Santo. species of animals are already regionally extinct Prince Maximilian also described a variety of (Passamani et al. 2007). These numbers are based environments and plant formations, including on assessments carried out in 2004 and therefore more than one type of forest, savannas (possibly the flora and fauna of Espírito Santo are likely to areas of restinga - vegetation on sandy soils be even more threatened today. along the coast in Brazil, and muçununga - low Currently, understanding how the loss of forests on sandy soils far from beaches), native species may contribute to the loss of ecological grasslands, swamps and lakes. These formations interactions, and vice versa, in the state of are encountered along the gradient from the Espírito Santo (and elsewhere) is limited due coastal region to the highlands and mountains. to the lack, and complexity, of studies of these The forests received most of his descriptive effects. Nonetheless, some general patterns attention, which he described at great length are understood, by which we can predict and as imposing and sombre, thick and beautiful or recognize consequences of the loss of species and simply grand and magnificent, with majestic trees interactions. Thus, here we review the literature that gave refuge to the abundant and extraordinary and place that in the context of Espírito Santo diversity of animals (Wied-Neuwied 1942). For and the Atlantic Forest to explain how the loss of details on the vegetation of the state of Espírito fauna can break down plant–animal interactions Santo, see Garbin et al. (2017). and result in the further loss of species and of The Espírito Santo that Wied-Neuwied interactions. We concentrate on the animals most visited he described as having “delightful often involved in pollination and seed dispersal landscapes” and “such superb scenes and so and that are found in the state of Espírito Santo. rich with notable specimens” that “naturalists We describe how different factors can cause will have a long time to occupy themselves,” vulnerability and local extinction of these with “the most varied and agreeable emotions” animals, as well as their ecological functions (Wied-Neuwied 1942). Even though the state and the plants with which they interact. This was largely unpopulated at the time, plantations manuscript is organized in the following sections: were already present (some of them extensive), Espírito Santo at the time of the early traveler especially of sugarcane, cotton, coffee, cassava naturalists, The process of occupation and and corn, that replaced the forests along the Espírito Santo today, Plant-animal interactions, coastal lowlands, along with some cattle rearing. The Insects, The Birds, The Mammals, and Final The forests in Espírito Santo were replete with a Considerations. variety of high-quality hardwoods that were being
Rodriguésia 68(5): 2001-2017. 2017 Defaunation triggers the loss of plant species 2003 exploited throughout the state for their lucrative diversity suffered from a variety of problems lumber. In addition to this early deforestation and that were (and are) caused by habitat loss and exploitation of forest resources, prince Maximilian fragmentation, and hunting that began with wrote of hunting wild game for food deep in the colonization and continues today. forests, using gunpowder and lead with shotguns, occasionally with hunting dogs to take large game The process of occupation that tended to avoid men. He described several and Espírito Santo today occasions in which the hunters returned home Today, the landscape of Espírito Santo is with bags or canoes nearly overloaded with game much different from that explored by the traveling that was so abundant in the local forests (Wied- naturalists of the 19th century. The economy of Neuwied 1942). the state continued to be dominated by sugarcane In 1860, the emperor Dom Pedro II visited and cassava, until coffee became more important, the territory of Espírito Santo and he wrote briefly beginning in the mid 1800s. Most of the settlements of his travels, with a little information on the flora. were located near the coast (did not extend beyond He wrote most about the natural environments 20 km inland) and the state was essentially (beaches, rivers, lakes) and fauna. Dom Pedro economically unexplored (Franceschetto 2014). II wrote, for example, about the extraordinary At that time, agricultural, especially plantations birdlife he found in the state, describing species for growing coffee, began to grow and spread of colorful and beautiful plumages, aquatic birds, westward (Loureiro 2006; Franceschetto 2014). hawks and others (Rocha 2008). He also wrote Until that time, Espírito Santo was viewed by the about the hunting for animal skins, including Portuguese Crown as a barrier that limited access to caimans, tapirs, capybaras, deer, anteaters and the state of Minas Gerais and which helped prevent jaguars (Rocha 2008). smuggling from that state (which was already The princess Teresa da Baviera, during a important for mining gold and precious stones). visit to Espírito Santo in 1888, also described Thus, before agricultural growth, the mountains, the fauna and flora of the state (in her writings along with the forest cover and the indigenous “Viagem ao Espírito Santo”). In addition to her peoples that resisted colonization, all contributed interest in the fauna and flora, princess Teresa to the delay in occupation of the interior of the state was fascinated by the habits and customs of the of Espírito Santo (Loureiro 2006; Franceschetto indigenous people of Espírito Santo, especially the Botocudos (indigenous groups of the Macro-Jê 2014). Often, lumber extraction preceded the ethnic group, that pierced their lips and earlobes establishment of the coffee plantations that in and inserted wooden discs with a diameter of up turn grew even more to increase production, and to 12 centimeters). She described her knowledge were subsequently abandoned when the soil was of nature as having been enriched by culinary no longer productive and which were replaced by experiences (animals that were hunted for food), pasture for the growing cattle industry. In some along with what she was taught by the indigenous places, economic activity began with logging of people and colonists (Baviera 2013). Princess high quality lumber and was followed immediately Teresa wrote of dining on a wide variety of by extensive cattle production (Loureiro 2006). animals, including insects, fish, reptiles (caiman, Espírito Santo continued its agrarian economy that snakes, lizards and sea turtle meat and eggs), birds was strongly dependent on the coffee monoculture (curassows and parrots, among many others) and until the late 1960s, when industrial activities began mammals (spotted pacas, deer, tapirs and big cats, to increase in importance, along with silviculture among others). Tapirs are emphasized and appeared (mainly eucalyptus) for the production of charcoal to be the most appreciated meat by the colonists in and cellulose for paper (Loureiro 2006). some parts of the state. In addition to their meat, As economic activities increased in the they were hunted for their hides as well, which state with the drive for additional development, was valuable at that time and used in a variety of deforestation continued rapidly as any arable applications (Baviera 2013). land in the natural environments was converted to These and other early traveling naturalists agriculture, silviculture and livestock. This state describe the beginning of the gradual and that was original completely covered by the Atlantic irreversible process that has lead up to the current Forest and its associated formations gave way to situation of decline and loss of wildlife in the state economic development. Less than 13% of the of Espírito Santo. Habitat integrity and species original natural areas remain, counting fragments
Rodriguésia 68(5): 2001-2017. 2017 2004 Srbek-Araujo AC et al. larger than 3 ha, which now comprises forest due to their relevance for 1) plant reproduction and (~11%) and non-forested natural areas (~2%), such maintenance of plant genetic diversity, affecting as seasonally flooded areas (várzeas), restingas reproductive success and plant fitness through and mangroves (FSOSMA & INPE 2016). As the pollination (Paschke et al. 2002) and 2) seed Atlantic Forest of Espírito Santo became more and germination and recruitment of seedlings, through more fragmented, most of the native fauna became seed dispersal that reduces density-dependent seed confined to the ever-smaller and more isolated predation near the parent plant (Janzen 1970). forest fragments. These smaller populations are In addition to ecological relevance, pollination beset by a variety of problems that reduce their and seed-dispersal comprise a very wide diversity chances of long-term survival along with that of of organisms, both plant and animal, and the loss of the ecological processes of which they are often a these interactions will result in a substantial loss of very important part. In addition to those biological biodiversity. For example, ca. 87% of angiosperms issues, climate change (changes in temperature, worldwide are pollinated by animals, and in precipitation, albedo and local microclimate), in the tropics increases to ca. 94% (Ollerton et al. part caused by deforestation, has consequences for 2011). Seed dispersal by animals is also extremely the remaining flora and fauna (Davies et al. 2001). important, especially in tropical forests where more The loss of animals due to poaching and roadkills, than 75% of trees species produce fruit whose and the introduction of exotic species, among other function is to attract animals so that they disperse anthropic factors, further aggravate the wildlife seeds (Howe & Smallwood 1982), including birds conservation scenario in Espírito Santo (e.g., and mammals, as well as reptiles, fish and ants. Passamani et al. 2007; Srbek-Araujo et al. 2014). Overall, in the Atlantic Forest about 65% of all woody plants are dispersed by vertebrates, as with Plant-animal interactions endozoochory (after being consumed along with The first scientific research carried out with fruit, seeds are regurgitated or defecated), while respect to plant-animal interactions is attributed in some places up to 90% are animal-dispersed, to Joseph Gottlieb Kölreuter, around 1760, with and so the loss of dispersers is likely to have the documentation of pollination service provided far-reaching effects (Almeida-Neto et al. 2008). by several insects. He was followed by Christian Plants that depend upon vertebrates for pollination Konrad Sprengel, in 1793, studying the relationship and seed dispersal will suffer both ecological and between plant fertilization and insects (Bascompte evolutionary consequences due to the loss of fauna & Jordano 2014). Among other researchers, plant- (genetic structure of populations can change, for animal interactions were also mentioned by Charles example), and in addition can reduce or eliminate Darwin, a hundred years later, in his monumental ecosystem services that these interactions provide “On the Origin of Species by Means of Natural (Galetti & Dirzo 2013). Defaunation of wildlife in Selection, or the Preservation of Favoured Races tropical forests, therefore, can result in a cascade of in the Struggle for Life”. Darwin point out that deleterious consequences for the entire community plants and animals are linked together and form a which causes the reduction in species richness and web of complex relations (Darwin 1859). Today greater dominance by a very few species, resulting we recognize (aside from foraging, such as seed in reduced biodiversity at all levels (Kurten 2013). predation and herbivory) four kinds of animal- plant interactions that are multispecies mutualisms: The Insects 1) pollination, 2) seed dispersal, 3) protective Insect pollination is very widespread in mutualisms or harvest mutualisms (comprising angiosperms and thus pollination is the more protection of plants by arthropods, especially ants, important mutualistic interaction between insects in exchange for some product the plants provide), and plants. A greater part of plant species in and 4) agriculture by humans (modified from tropical forests are pollinated by insects, and Bascompte & Jordano 2014). several groups of insects stand out as pollinators, In this study, we will focus on pollination including Coleoptera (beetles), Diptera (flies), and seed dispersal to explain how the loss of Hymenoptera (bees and wasps) and Lepidoptera fauna can break down these two important plant- (butterflies and moths; Kevan & Baker 1983; animal interactions and result in the further loss Roubik 1989; Bawa 1990). of species (both plant and animal) in the state of The degree of specialization/generalization Espírito Santo. These interactions were selected of the interaction between plants and insects is
Rodriguésia 68(5): 2001-2017. 2017 Defaunation triggers the loss of plant species 2005 variable. It can be classified into four categories of families including Apocynaceae, Asteraceae, according to the functional groups of pollinators Bignoniaceae, Fabaceae, Melastomataceae, (beetles, syrphids, other dipterans, small bees, large Myrtaceae, Passifloraceae, Rosaceae, Rubiaceae, bees, wasps, and butterflies/moths), as: monophily Sapindaceae and Solanaceae (Marchi & Alves- (exclusively pollinated by one functional group), dos-Santos 2013). oligophily (two functional groups, and one or While we are more concerned with insect both are the main pollinators), polyphily (three pollination, due to the ubiquitous nature of ants or more functional groups, but only one or two in tropical forests, they merit at least a mention. groups are the main pollinators) and holophily (a Some ants do clean and disperse seeds of several variety of functional groups pollinate indistinctly) species of plants (Howe & Smallwood 1982; Pizo (Freitas & Sazima 2006). Usually the number of & Oliveira 2000), and other symbioses between functional groups of pollinators is strongly related ants and plants bear mention. Ants may defend to coevolution between certain groups of insects plants against herbivory and defended plants often and plants - fewer pollinators, greater likelihood have structures in which ants may feed (extrafloral of coevolution (Roubik 1989). nectarines) and live. Extrafloral nectarines are Bees and wasps (Hymenoptera) are the present in over one hundred of Angiosperm most important insect pollinators as measured by families worldwide, and the families with the most number and variety of plant species pollinated species with extrafloral nectarines are Fabaceae, as well as number and variety of hymenoptera Passifloraceae and Malvaceae (Weber & Keeler involved (Bawa 1990), especially small and large 2013). Many species of plants apparently have bees (Kevan & Baker 1983; Roubik1989; Freitas & adapted structures for the express purpose of being Sazima 2006; Senapathi et al. 2015). The majority inhabited by ants, such as the two well-known of species in some common plant families are examples of hollow stems occupied by ants in pollinated by bees in neotropical forests, including the genus Cecropia (family Urticaceae) and the Burseraceae, Clusiaceae, Euphorbiaceae, Fabaceae hollow thorns of some Fabaceae (Hölldobler & (Leguminoseae), Flacourtiaceae (currently Wilson 1990). reorganized as other botanic families, such as Ants have a great interaction with diaspores Achariaceae, Samydaceae and Salicaceae), of at least 30 families in the Atlantic Forest, Lecythidaceae, Melastomataceae, Orchidaceae and such as Annonaceae, Arecacea, Euphorbiaceae, Sapotaceae, including flowers of both the canopy Melastomataceae, Meliaceae, Myristicaceae, and understory (Bawa 1990). Several species Myrtaceae, Olacaceae, Sapotacea and Verbenaceae having monophily and oligophily are pollinated (Pizo & Oliveira 2000). Some species of small by bees (Roubik 1989; Freitas & Sazima 2006). and medium-sized ants fed on and cleaning the The orchid bees (tribe Euglossini) have fallen fleshy diaspores or occasionally transport long to extremely long tongues, and they visit a very small seeds, and the large ants (subfamily wide range of deep, tubular flowers that are not Ponerinae) individually moved diaspores (up to accessible to other bees (Dressler 1982). They 1 g, Pizo & Oliveira 2000). Even in cases where are important pollinators that visit flowers to the dispersion by ants can be considered low, their get their nectar, pollen, resin and (the males) to importance tends to be significantly higher in the collect aromatic chemicals that they then convert absence of primary dispersers (Brito-Kateivas to pheromones (Dressler 1982). Orchid bees are & Corrêa 2012). Ants can sometimes also act as known to visit flowers of around 30 families in pollinators, through the adhesion of pollen to hairy tropical and subtropical forests in Central and structures in their bodies (Beattie 1985). Because South America (Tonhasca Jr et al. 2003), including the ant-plant interactions are often overlooked, the Apocynaceae, Bignoniaceae, Convolvulaceae, consequences of fragmentation for both ants and Gesneriaceae, Marantaceae and Rubiaceae, and plants require further study. they are the only pollinators of some neotropical Abundance and species richness of insects Orchidaceae (Dressler 1982). tends to decrease with reduction in area of The mamangavas (bumble bees, genus the habitat and due to edge effects (change in Bombus, tribe Bombini; and carpenter bees, microclimatic conditions), and small, isolated genus Xylocopa, tribe Xylocopini) are large and fragments may also lack habitat heterogeneity robust bees. They are generalists bees and visit needed to support pollinator populations throughout flowers to collect pollen and nectar of a variety the year (Bawa 1990). Some groups, such as the
Rodriguésia 68(5): 2001-2017. 2017 2006 Srbek-Araujo AC et al. orchid bees, are dependent on well preserved forests as the addition of seed predators as well as reduced and are vulnerable to the loss of suitable habitat, reproductive success due to the loss of pollinators. and often disappear in small fragments (Nemésio The first step in understanding how 2011). Ant species richness and composition are fragmentation can result in the loss of important also influenced by fragment size and tree density, bird species that then contributes to plant extinction and some species are particularly sensitive to forest debts, requires understanding how habitat fragmentation (Leal et al. 2012). Many species and fragmentation is likely to influence, and reduce, groups of pollinators (principally bees), as well as bird populations. A reduction in bird populations the plants they pollinate, are negatively affected implies both abundance and species richness. Also, also by agricultural intensification (including the considering that the contribution of birds to the use of agrochemicals), diseases, invasive species maintenance of the plant community depends on the and climate change (Senapathi et al. 2015). species of birds and their foraging habits, we must Ecological changes, such as loss of pollinators, understand the dynamics of the different trophic can lead to pollen limitation that then reduces groups, especially frugivores. Also, population reproductive success of the plants, causing a decline dynamics depends on survival and reproduction in seed production (Ashman et al. 2004). The rates of the various species involved (Martin 1995), bumble bees, for example, are facing population and so we must look at how those dynamics will be declines and consequent decrease in pollination influenced by forest fragmentation (Martin 1996). service has already been documented around the Nest predation in natural settings is the cause world (Williams & Osborne 2009). Those factors of most reproductive failures (Ricklefs 1969; all together result in the decrease on community Skutch 1985; Roper et al. 2010). Thus, any changes stability by the disruption of mutualistic insect- in nest predation rates due to forest fragmentation plant interactions, highlighting the loss of one should have importance influences on population partner in species-specific interactions may lead to growth or decline. Studies demonstrate that nest the extinction of the other (Bawa 1990). Ecosystem predation rates tend to increase in fragmented integrity in a future of environmental change is landscape, usually because predators from outside essential in order to maintain not only pollination the fragment (such as feral cats, dogs, rats) find it services but also species diversity required to easier to enter well into the fragment (Sherry 1986; guarantee the functional redundancy and a range Newton 1993; Kays & DeWan 2004; Obrien et al. of reactions to environmental change (Senapathi 2008). Predation rate tends to be greater in tropical et al. 2015). forests and birds may lose up to and more than ~90% of their nesting attempts due to predation The Birds (Roper 2005; Roper et al. 2010). Dynamics of Habitat fragmentation can initiate a variety reproduction and adult longevity may maintain a of snowball effects of changes in their animal and population, but if faced with even small changes plant communities. For example, some species of in either reproductive success or adult survival, birds are rapidly lost after fragmentation and some population decline may follow rapidly. may quickly and others more slowly return upon Small and medium-sized predators that are forest recovery. Also, species loss and recovery associated with humans (cats, dogs, rats) may often are both functions of the size of the fragment and become more important with fragmentation because their distance from source populations as well as of the increase in edge and decrease in forest the autecology of the species of interest (Stouffer interior. Additionally, smaller natural predators can & Bierregaard 1995; Ferraz et al. 2003; Stouffer become more abundant due to the decline of the et al. 2011). Here we are concerned with the larger predators in fragments (Sodhi et al. 2004). ways in which fragmentation can influence the Thus, species with relatively stable populations and bird assemblage which, in turn, influences the that tend to suffer higher predation rates may be plant species that persist or invade the fragments. faced with greater predation rates, that then cause While an extinction debt occurs after habitat their population declines. For example, in Panamá, fragmentation, in which species loss continues over Thamnophilus atrinucha Salvin & Godman, 1892 time (Tilman et al. 1994), we must recognize that (family Thamnophilidae, with several similar the loss of plant species can depend on the dynamics species in Espírito Santo) loses 89% of its nesting due to a variety of interactions, including reduced attempts to predation (Roper 2005). However, due seed dispersal due to the loss of frugivores as well to seasonality in eastern Brazil, the breeding season
Rodriguésia 68(5): 2001-2017. 2017 Defaunation triggers the loss of plant species 2007 is probably much shorter in Espírito Santo and an and the bem-te-vi (Great Kiskadee, Pitangus increase in predation to similar rates is likely to sulfuratus (Linnaeus 1766) and similar species) cause population decline (Roper et al. 2010). The and a variety of lesser known understory and exact dynamics of fragmentation, edge effect and forest species. The Cotingidae tend to be extremely changes in survival and predation rates continue specialized in frugivory and include the araponga to be debated (Flaspohler et al. 2001; Lloyd et al. (bellbirds, genus Procnias) among others. The more 2005, 2006; Rush & Stutchbury 2008; Bueno et al. omnivorous Tityridae (until recently considered 2012); nonetheless, evidence and logic suggest that Cotingidae) includes the anambé (tityras, genus small changes in survival and reproduction can have Tityra) and caneleiros (genus Pachyramphus). dramatic deleterious effects on bird persistence. The frugivore family Pipridae includes a variety Therefore, changes in species composition of of smaller species that form leks in which the fragments are expected as fragmentation increases males gather in groups to dance in fascinating and fragment size decreases. coordinated cooperation to gain the attention The exact relationship of species changes of the females (genus Pipra, among others, and over time with fragmentation is, of course, some species of smaller Tyrannidae also do this, influenced by the niches of the species involved. and they tend to be frugivorous as well). Also Most studies about nesting success have included omnivorous, the Thraupidae comprise a colorful territorial, insectivorous species that are easier to family of birds, including the well-known tiê- study precisely due to their territoriality (Robinson sangue (genus Ramphocelus, and others). The et al. 2000; Duca & Gonçalves 2001; Wikelski well known sabiás (thrushes, family Turdidae) are et al. 2003; Roper 2005; Duca et al. 2006; Duca omnivorous and extremely common and consume & Marini 2011, 2014; Marques-Santos et al. fruits of both native and exotic plant species 2015; Lima & Roper 2016; Mathias & Duca (Ridgely & Tudor 1989a; Ridgely & Tudor 1989b). 2016). While insectivorous birds may influence Thus, we find a wide range of breeding and social plant species through predation on herbivorous systems and feeding ecologies among several bird insects, plant dynamics will be more strongly families, all of which will be influenced by forest influenced by birds that pollinate plants and that fragmentation. We can divide these frugivores into disperse seeds. Population dynamics are much two main groups: the larger birds including the less studied in frugivores (families Cracidae, curassows and guans, that may be very efficient Tyrannidae, Cotingidae, Pipridae and Thraupidae, seed disperses that tend to prefer forests and which with Turdidae somewhat of an exception) and will suffer from nest predation as well as poaching pollinators (hummingbirds, family Trochilidae). in fragmented landscape; the remainder being the Many of these species nest similarly to the more smaller birds whose survival patterns in fragments studied insectivores, and we must assume that are not easy to predict, but whose breeding patterns predation on their nests will have similar trends should be influenced by increasing nest predation in fragmented habitats. However, these groups in fragments. However, the smaller birds include comprise a wide range of autecologies and body the thrushes (sabiás in Brazil, family Turdidae) size, all of which will have consequences on that have become associated with urban and rural dynamics in fragmented environments. In general, landscapes and which seem to have characteristics large species tend to have slower reproductive rates that allow them to do well in anthropic settings and longer intervals between breeding attempts (about which more below). than the faster, smaller species (Robinson et al. Large birds, such as the curassows and guans, 2010; Lovette & Fitzpatrick 2016). also suffer from both predation and poaching Frugivorous birds comprise a wide variety (Michalski & Peres 2005, 2007; Barlow et al. 2006) of ecologies in eastern Brazil, beginning with the and are likely to disappear rapidly from fragments large curassows and guans (familia Cracidae) that (Harris & Pimm 2008). Because they are large, they may often be important seed dispersers (Terborgh can also consume larger fruits, often entirely, and et al. 1990; Marini 2001; Pimm et al. 2006; Kirwan thereby carry their seeds (disperse) longer distances 2009). Smaller frugivores include families that are where they will be defecated. Breeding rates tend common in Espírito Santo and are often birds of to be relatively slow with extended intervals of urban and rural regions. The Tyrannidae include parental care. Thus, potential population growth the well-known suiriris (kingbirds and similar is relatively slow and after fragmentation is likely species, in the genera Tyrannus and Myiarchus) to decline. As a consequence, the species of plants
Rodriguésia 68(5): 2001-2017. 2017 2008 Srbek-Araujo AC et al. that depend upon these dispersers may have no they may have more than one success per year counterparts among the smaller frugivores of (Marini et al. 2012; Marques-Santos et al. 2015). the forest, much like the extinct megafauna on Unfortunately, also do their generalist habits, a smaller scale (Janzen & Martin 1982). These these species may often contribute to diversity birds also need relatively large areas to support homogenization (Elton 2000; Crooks 2004; Qian stable populations (Sodhi et al. 2004; Bernardo et & Ricklefs 2006; Babak & He 2008; Croci et al. al. 2011). Thus, following fragmentation, reduced 2008; Winter et al. 2009; Gossner et al. 2016) populations due to fragmentation will be followed because they consume fruits of exotic species as by continuing population decline, which is likely well as native species, dispersing seeds for both to result in dispersal limitation for any species groups. As a consequence, due to the extinction dependent upon these large birds (Freestone debt, exotics may become much more abundant & Inouye 2006; Moore et al. 2008; Pinto & than native species. As the exotics become more Macdougall 2010). abundant, omnivorous birds may benefit, while the The extreme frugivores (family Cotingidae) more extreme frugivores may not, thereby further tend to produce very small clutches and the contributing to their decline as well as their role in bellbirds (arapongas, genus Procnias) only lay the maintenance of the plant community. one egg per nest. Also, the young require a very The threat to plant communities through long time interval to leave the nest and these two the loss or decline in their seed dispersers is patterns together, perhaps due to frugivory, tend clearly an important threat for tropical forests as to result in very slow potential population growth a consequence of forest fragmentation. However, (Snow & Goodwin 1974; Ingels 2008; Kirwan & an equally important process may be less obvious Green 2011). The manakins (dançarinos, family and that is of the pollinating species that help Pipridae) only lay two eggs per nesting attempt, but maintain genetic diversity of plant populations. may have several nesting attempts per year, and so Hummingbirds (beija-flores, family Trochilidae) their potential for population growth is greater than comprise a diverse group of birds with one thing that of the bellbirds. Both of these birds families are in common - they all visit and pollinate plants. very important seed dispersers because they often Many species of hummingbirds migrate and consume entire fruits and regurgitate or defecate local migration may often occur as the timing the seeds (perhaps gaining a germination benefit of flowering changes among the many species in the process, Calviño-Cancela 2004; Daïnou et of plants that they visit (Wethington & Russell al. 2012) long distances from where they were 2003; Arizmendi & Ornelas 2007). Mostly due consumed (Snow & Goodwin 1974; Kirwan & to their small size, hummingbirds are poorly Green 2011). These species are also likely to studied and the impact of their pollination on decline in fragments, in part to the extinction plant reproductive success is hard to estimate. debt (Tilman et al. 1994) that will result in the However, the very strong coevolutionary patterns disappearance of some species of fruiting plants, of the New World Hummingbirds (Cotton 1998; as well as to slow reproductive rates coupled with Zanata et al. 2017) suggest that hummingbirds increased nest predation. The tanagers (family have been extremely important in the evolution and Thraupidae) and flycatchers (Tyrannidae) include diversity of tropical plants. The state of Espírito some species with similar life histories that will be Santo has about 33 species of hummingbirds that affected similarly, resulting in a general decline in range in size from ~2–9 g, with short to long bills richness of seed dispersing species. Some species, and that inhabit a variety of habitat types (Ruschi nonetheless, seem to benefit from fragmentation. 1982; Ridgely et al. 2015). Despite their species Several species of tanagers and flycatchers, diversity and behavior as pollinators, the difficulty but especially the thrushes (family Turdidae), seem of studying how plants depend on their pollinators to benefit from fragmentation, perhaps because has impeded the understanding of the importance they have always been associated with marginal of hummingbirds for the persistence of the plants habitats. These species also tend to be omnivorous they pollinate. Also, because hummingbirds are so and consume a wide variety of resources (Ridgely small and often difficult to detect within forest, how & Tudor 1989a, 1989b; Sick 1993). Also, many fragmentation influences their own populations species in this group are habitat generalists and are remains unknown. Nonetheless, the existing able to nest in a variety of settings. Reproductive evidence suggests that plants benefit from the plant rates are also more rapid among these species, and hummingbird association, but that hummingbirds
Rodriguésia 68(5): 2001-2017. 2017 Defaunation triggers the loss of plant species 2009 themselves may be less affected by fragmentation precarious position in forest fragments, are also if fragments are larger than 10 ha and relatively subject to poaching, adding additional pressures near much larger forest fragments (Borgella et al. that can drive them to local extinction in the 2001; Martín González et al. 2015). Atlantic Forest (Chiarello 1999; Galetti et al. 2009; Sousa & Srbek-Araujo 2017). The Mammals The ability of any species to withstand Bats landscape modifications is determined by how Bats (order Chiroptera) form a very diverse much habitat is loss, how isolated the resultant group and which, because of their food habits, fragments are and how strong is the rupture in have ecological functions that are fundamental to biological and interspecific interactions of which the maintenance of plant communities (Charles- the organisms play a part (Fischer & Lindenmayer Dominique 1986; Fenton et al. 1992; Fleming & 2007). In general, mammals are susceptible to Sosa 1994). Bats and plants have a very strong habitat fragmentation and its effects on the species interaction and when bats consume fruits, nectar or depend on not only size and degree of isolation of pollen, they provide seed dispersal and pollination the fragments, but also the spatial arrangement of in exchange for the nutrients the plants provide. fragments in the landscape (Andrén 1994). Even Thus, the association between many plants and species that are very mobile can suffer from the bats is often exclusive, and some plant species effects of isolation in very fragmented landscapes, have clearly coevolved with bats for seed dispersal and it is unlikely that isolated, relatively small (chiropterocory) and pollination (chiropterophily, (few hectares) fragments can maintain mammal Hilje et al. 2015). populations (Andrén 1994). Thus, the composition Bats are among the most efficient mammalian of the matrix (the area between fragments), along seed dispersers (Fleming & Sosa 1994), in part with the dispersal capacity of the species of interest, because they are the only truly volant mammal and its ability to move from one fragment to another or in part because they are so abundant and varied to live in the matrix, are elements that will define in their use of resources and habitat within any the vulnerability of that species to fragmentation landscape (Estrada et al. 1993). It is estimated that and habitat loss (Fischer & Lindenmayer 2007). a 145 g bat can disperse thousands of seeds in a Mammals with restricted geographical single night (Esbérard 2000), often carrying seeds distributions, low population density, low large distances from the parent plant (Morrison reproductive rates, large body size and that 1980; Charles-Dominique 1986). The size of occupy higher trophic levels tend to be the most seeds that bats disperse varies widely. Smaller vulnerable to extinction (Purvis et al. 2000). For seeds are dispersed by endozoochory (ingested the ecosystem, the consequences of species loss and eliminated with feces) while larger seeds are will depend upon redundancy of the species in the dispersed by stomatochory (carried to a feeding system. Where a variety of species serve the same perch where the bat will consume the fruit pulp function, the loss of any one element may not be and drop the seed). immediately apparent, but when few or no species Bats in the family Phyllostomidae, especially are redundant, the loss of the keystone species those in the subfamilies Stenodermatinae, can then cause an important loss in functional Carolliinae and Rhinophyllinae, are specialized in diversity (Petchey & Gaston 2002). This pattern frugivory in the neotropics (Reis et al. 2007; Lima is especially important for larger species (Brose et et al. 2016). In the Atlantic Forest of the state of al. 2017). Larger mammal species tend to interact São Paulo these bats are known to disperse seeds (consume, predate, disperse) with a larger number of at least nine genera of native plants in eight of plant species and, consequently, the loss of the plant families (Passos et al. 2003). In Espírito large mammal can result in the simplification of Santo, bats disperse at least 20 native plants in trophic networks (Brose et al. 2017). 15 genera and 13 families (Zortéa & Chiarello Here we will discuss only bats and medium 1994; Pedro & Passos 1995; Lima et al. 2016). to large-sized mammals because both groups Families dispersed by bats in the two states include are known to play important parts in plant- Araceae, Clusiaceae, Curcubitaceae, Moraceae, animal interactions in tropical forests, especially Piperaceae, Solanaceae and Urticaceae (Zortéa & pollination and seed dispersal. The medium Chiarello 1994; Pedro & Passos 1995; Passos et to large-sized mammals, in addition to their al. 2003; Lima et al. 2016). Additional families
Rodriguésia 68(5): 2001-2017. 2017 2010 Srbek-Araujo AC et al. dispersed by bats include Rosaceae, in the state of Sazima et al. 1999; and Phyllostominae, Silva & São Paulo (Passos et al. 2003), and Humiriaceae, Peracchi 1995). A variety of plants are pollinated Lauraceae, Fabaceae, Malpighiaceae, Myrtaceae by bats (Sazima et al. 1982; Sazima & Sazima and Passifloraceae, in the state of Espírito Santo 1988; Silva & Peracchi 1995; Sazima et al. 1999; (Zortéa & Chiarello 1994; Lima et al. 2016). The Arias et al. 2009; Ramírez et al. 2015), many first records of bats (Artibeus lituratus (Olfers, of which evolved flowers that favor pollination 1818)) carrying fruits of the muçununga-endemic by bats (Howell 1974). Flower adaptations that Humiriastrum mussunungense Cuatrec were noted favor bats including nocturnal anthesis (flower in Espírito Santo (Lima et al. 2016). Muçununga opening), white or light colored petals in flowers is a forest formation unique to sandy soils in the located towards the ends of branches and oriented Atlantic Forest in the northern Espírito Santo and in such a way as to facilitate bat visits and contact southern Bahia. with pollen, as well as having particular odors and The most commonly observed genera of production of larger amounts of pollen and nectar fruits being consumed by bats include Ficus, (Howell 1974; Ramíres et al. 2015). Cecropia, Piper, Solanum and Vismia (Mikich et Studies of plant species pollinated by bats al. 2015). Some bat genera seem to be strongly are still few in the Atlantic Forest. Nonetheless, associated with particular groups of plants, bats in the subfamily Glossophaginae have been such as Artibeus spp. with Ficus and Cecropia, found to pollinate at least 19 plant genera in this Sturnira spp. with Solanum, and Carollia spp. biome (Nogueira et al. 2007). In the state of São with Piper (Pedro & Passos 1995; Passos et al. Paulo, for example, 16 species in 10 genera and 2003; Mikich et al. 2015). This specialization is 10 families were pollinated by bats (Sazima et al. apparently associated with resource partitioning 1999). Among the more important pollinating bats in which similar sympatric species avoid or reduce are Glossophaga soricina (Pallas 1766) that is competition thereby allowing species coexistence important in pollinating two Atlantic Forest endemic (Marinho-Filho 1991). These plant species are plants, Dyssochroma viridiflorum (Sims) Miers (an often associated with secondary succession in epiphytic Solanaceae) and Pitcairnia albiflos Herb disturbed or damaged areas, and bats tend to (a rare bromeliad of the Tijuca Forest in the state of disperse seeds during flight into altered areas (seed Rio de Janeiro) (Nogueira et al. 2007). rain), thereby contributing to forest regeneration Fragmentation is usually accompanied by (Charles-Dominique 1986; Martins et al. 2014). the loss of bat species, including dispersers and In Espírito Santo, 60% of bat-dispersed plant pollinators, because some species of bats are very species are of early successional stages, three sensitive to loss of habitats and often may not visit genera of which are pioneers and another six are isolated forest patches (Fenton et al. 1992; Fuchs from early stages of secondary succession (Lima et al. 2003). For these species, the matrix between et al. 2016). Bats can also disperse seeds of exotic fragments becomes an effective bat filter (Cosson et species (Zortéa & Chiarello 1994; Lima et al. al. 1999). Thus, smaller bats and those of the forest 2016), thereby contributing to plant invasions and interior are even more sensitive to fragmentation species homogenization (e.g., Qian & Ricklefs and their loss or isolation in fragments can have 2006; Winter et al. 2009). For example, in Espírito demographic consequences for the plants they visit Santo, Artibeus spp. disperse seeds of exotic plants and disperse (Cosson et al. 1999). As pollinators, in the families Arecaceae, Rosaceae (Zortéa & it has been shown that at least one species of Chiarello 1994), Fabaceae (Lima et al. 2016) and bat-pollinated plants produced a lower fruit set Sapotaceae (A.C. Srbek-Araujo, unpublished data). (number of fruits per flower produced in each Some bats are also effective pollinators tree) in fragments than in continuous populations, (Fleming & Sosa 1994) and the neotropical suggesting that the loss of or reduction in pollinator Phyllostomidae, subfamily Glossophaginae, activity can often reduce the fitness of their include species specialized for pollination. These host plants (Fuchs et al. 2003). Additionally, in species tend to have morphological adaptations for continuous populations, progeny had lower levels of feeding in flowers, including an exceptionally long relatedness due to greater outcrossing or more sires tongue and a long snout (Silva & Peracchi 1995). (Fuchs et al. 2003). Thus, fragmentation can simply Other Phyllostomidae species are less specialized, make it harder for plants to be found by their bat but also visit flowers and may be occasional pollinators, thereby reducing reproductive output pollinators as well (subfamilies Stenodermatinae, of those plants which then becomes a vicious cycle.
Rodriguésia 68(5): 2001-2017. 2017 Defaunation triggers the loss of plant species 2011 Medium and large-sized mammals pattern of movement, habitat use and social Among the medium and large-sized mammals organization (Bueno et al. 2013). Thus, seed that were or are common in the Atlantic Forest and dispersal is complementary rather than redundant important for plant-animal interactions, are primates among medium and large-sized mammals (Bueno (family Atelidae: genus Alouatta - howler monkeys, et al. 2013), and complements patterns of birds and genus Brachyteles - muriquis, formerly wooly- and bats. For example, tapirs and muriquis have spider monkeys; and family Cebidae: genus Sapajus distinct seed dispersal effectiveness and disperse - capuchin monkeys), medium-sized rodents a variety of plant species, some of which are (family Dasyproctidae: genus Dasyprocta - agoutis; dispersed by both or by one or the other (Bueno et and family Cuniculidae: Cuniculus paca (Linnaeus, al. 2013). According to compiled information from 1766) - spotted paca), squirrels (family Sciuridae: a literature review, tapirs are known to disperse genus Guerlinguetus) and ungulates (order seeds from at least 34 plant families (76 species), Artiodactyla, family Tayassuidae: Pecari tajacu muiriquis disperse 55 families (220 species) and (Linnaeus 1758) - collared peccary, and Tayassu their overlap includes 24 families (29 species) pecari (Link 1795) - white-lipped peccary; and (Bueno et al. 2013). the order Perissodactyla, family Tapiridae: Tapirus Several plant families are dispersed by terrestris (Linnaeus 1758) - lowland tapir). Some medium and large mammals and include the species in the order Carnivora, especially in the important families Anacardiaceae, Arecaceae, families Canidae (dogs and foxes) and Procyonidae Annonaceae, Celastraceae, Chrysobalanaceae, (coati, kinkajou and raccoon), also often consume Euphorbiaceae, Fabaceae, Lauraceae, fruits and disperse seeds. These mammals act as Malphigiaceae, Melastomataceae, Moraceae, primary and/or secondary seed dispersers, some of Myrtaceae, Rubiaceae and Sapotaceae, along which may often be seed predators as well (Gautier- with many others in the Atlantic Forest (Hilje Hion et al. 1985; Kurten 2013). Additionally, the et al. 2015; Bueno et al. 2013). Thus, the loss rodents are also important for their habit of scatter- of larger mammals can completely change the hoarding or caching seeds (Gautier-Hion et al. dynamics of dispersal for many species in these 1985; Kurten 2013), which effectively disperses (and other) families, thereby potentially altering the seeds in a variety of different places, often community composition and genetic structure leading to germination. Medium and large-sized of the populations. Also, the absence of large mammals often defecate the ingested seeds mixed frugivores may result in greater seed predation with various amounts of fecal matter, which may rate (up to five times more) due to the predation by create an ideal environment for germination, aside small rodents (Galetti et al. 2015). Although small from the possible benefits of seed processing by rodents can disperse seeds, they are responsible passing through the gut of the animal. for consuming about 64% of all seeds in non- Larger frugivorous mammals are not simply defaunated sites, and more than 98% in defaunated redundant in terms of their importance for seed areas (sites where large mammalian herbivores dispersion with respect to bats and birds. These were extirpated, Galetti et al. 2015). mammals often eat larger fruits and those with In Espírito Santo, larger frugivores have tough pericarps that are not accessible to other declined in abundance and often disappeared seed dispersers. The rodents with their specialized completely from many forest fragments and incisors and the primates with their visual acuity therefore, most of the state. For example, red- and ability to manipulate can harvest kinds of rumped agoutis (Dasyprocta leporina (Linnaeus fruits that birds and bats cannot. Also, ungulates 1758) were once common throughout the state, can swallow larger seeds rather than crush all them and are still relatively common in some protected with their molariform teeth. Additionally, some areas, but they have disappeared from many smaller of the larger mammals tend to remove a larger fragments and elsewhere are in decline or are less number of seeds and, due to the size of their home abundant than they once were (Chiarello 1999). ranges, they disperse seeds over larger distances A similar, but more extreme, trend is found in the (Fragoso et al. 2003; Bueno et al. 2013). Seed spotted pacas (Chiarello 1999) and they remain dispersal by medium and large-sized mammals is one of the most favored illegally-hunted prey in variable quantitatively, qualitatively and spatially, Espírito Santo (Chiarello 1999; Sousa & Srbek- and is influenced by gut passage time, defecation Araujo 2017). The northern muriqui (Brachyteles frequency, defecation behavior (e.g., latrine use), hypoxanthus (Kuhl 1820)), found only in the
Rodriguésia 68(5): 2001-2017. 2017 2012 Srbek-Araujo AC et al. mountainous regions, today is restricted to two be exotic) and the very limited number of pollinator protected areas and very few small fragments and seed-dispersing species that can be supported on private land in the state (Mendes et al. 2008). by them (Elton 2000). We are going to experience a Lowland tapirs, once found throughout the state, synergistic decline in fauna and flora components, are restricted to only three regions in the north with the simplification of biological communities (Flesher & Gatti 2010), two of which include the and the loss of ecosystem services provided by last populations of the white-lipped peccary in animals and plants. Espírito Santo (Chiarello 1999). Larger mammals We recommend that studies be carried out to clearly face a much greater challenge to their map the ecological interactions between animals continued survival in the state, and all suffer from and plants in Espírito Santo (and elsewhere), to forest fragmentation, habitat loss and poaching. better understand the consequences of and synergy The impact of their decline as seed dispersers between their losses, to extend what is known for the many plant species associated with them beyond general theoretical patterns. Conservation is very difficult to predict. Nonetheless, the loss efforts must reduce the impact of fragmentation of large frugivores is of such importance that the before the harm is irreparable, and to restore ecosystem services they provide are failing and interactions when possible to recover the original probably already lost in many places. 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Editora de área: Dra. Tatiana Carrijo Artigo recebido em 16/06/2017. Aceito para publicação em 30/10/2017.
Rodriguésia 68(5): 2001-2017. 2017